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Biol Invasions (2010) 12:1591–1605
DOI 10.1007/s10530-009-9572-7
ORIGINAL PAPER
Distribution and community-level effects of the Chinese
mystery snail (Bellamya chinensis) in northern Wisconsin
lakes
Christopher T. Solomon Æ Julian D. Olden Æ
Pieter T. J. Johnson Æ Robert T. Dillon Jr. Æ
M. Jake Vander Zanden
Received: 20 November 2008 / Accepted: 24 August 2009 / Published online: 10 September 2009
Ó Springer Science+Business Media B.V. 2009
Abstract Managing invasive species requires information about their distributions and potential effects,
but community-level impacts of invasive animals
remain poorly understood. The Chinese mystery snail
(Bellamya chinensis) is a large invasive gastropod that
achieves high densities in waters across North America, yet little is known about its ecological significance
in invaded systems. We surveyed 44 lakes to describe
the patterns and determinants of B. chinensis distributions in northern Wisconsin, USA, and to assess the
likelihood of effects on native snail communities in the
invaded systems. B. chinensis was widespread among
Electronic supplementary material The online version of
this article (doi:10.1007/s10530-009-9572-7) contains
supplementary material, which is available to authorized users.
C. T. Solomon (&) M. J. Vander Zanden
Center for Limnology, University of Wisconsin, 680 N.
Park St., Madison, WI 53706, USA
e-mail: [email protected]
surveyed lakes (21 of 42 lakes with snails) and its
occurrence was correlated with indicators of lake
productivity and anthropogenic dispersal vectors (boat
landings, distance to population centers, shoreline
housing density). Some native snail species tended not
to occur at sites where B. chinensis was abundant;
among these was Lymnaea stagnalis, which suffered
reduced survival in the presence of B. chinensis in a
recently published mesocosm study. However, there
was no difference in overall snail assemblage structure
at either the site or lake level as a function of
B. chinensis presence or abundance. Lake occurrences
of many snail species have apparently been lost over
time, but a comparison to a 1930s survey showed that
there was no increased likelihood of species loss in
lakes invaded by B. chinensis (or by the invasive
crayfish Orconectes rusticus). Although B. chinensis is
widespread and sometimes abundant in northern
Wisconsin lakes, it does not appear to have strong
systematic impacts on native snail assemblages.
J. D. Olden
School of Aquatic and Fishery Sciences, University
of Washington, Box 355020, Seattle, WA 98195, USA
Keywords Gastropoda Viviparidae Biogeography Cipangopaludina Bellamya japonica
P. T. J. Johnson
Department of Ecology and Evolutionary Biology,
University of Colorado, Ramaley N122, Campus Box 334,
Boulder, CO 80309, USA
Introduction
R. T. Dillon Jr.
Department of Biology, College of Charleston,
Charleston, SC 29424, USA
The ecological impacts of an invasive species are a
function of its range, abundance, and per-capita
effects, and may be manifested at levels of biological
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organization ranging from the genome to the ecosystem (Parker et al. 1999). For researchers and managers interested in conserving species diversity,
understanding impacts at the community level is
particularly important. An emerging consensus suggests that the risk of an invasive species causing
ecological change depends on the degree of functional similarity between that species and the native
species pool; distinctiveness of the invader enhances
its impact on native species (Ricciardi and Atkinson
2004), and competitors rarely cause extinctions,
whereas predators are more likely to do so (Davis
2003; Sax et al. 2007). However, there remains a high
level of taxonomic and geographic bias in the study
of invasive species (Pysek et al. 2008), and relatively
few studies have quantified the community-level
consequences of invasive animals (Parker et al.
1999).
Freshwater gastropod assemblages provide a useful and important model system for studying the
community-level effects of invasive competitors.
Field studies of gastropods show patterns consistent
with interspecific competition, and experimental
manipulations have demonstrated the importance of
interspecific resource competition and other negative
interactions within this group (Brown 1982; Hershey
1990; Adam and Lewis 1992; Turner et al. 2007; see
review in Dillon 2000). Furthermore, freshwater
gastropods are of significant conservation importance
because they are both highly diverse and highly
threatened (Lydeard et al. 2004; Strayer 2006; Lysne
et al. 2008). Concurrently, many gastropods have
become invasive; for instance, the United States
Geological Survey’s Nonindigenous Aquatic Species
database lists *40 invasive gastropod species in the
United States (http://nas.er.usgs.gov). Yet while some
invasive gastropods are known to have large effects
on invaded ecosystems (e.g., Hall et al. 2003;
Carlsson et al. 2004) or on particular native species
(e.g., Pointier and McCullough 1989), their community-level effects on potential competitors within the
snail assemblage remain relatively unexplored.
The Chinese mystery snail (Bellamya [=Cipangopaludina] chinensis (Reeve 1863)) is a viviparid
gastropod native to Asia. It is very large, reaching a
shell length of *65 mm and dry tissue mass of *1 g
(Jokinen 1982; Solomon unpubl. data). Its first
reported occurrence in North America was in a food
market in San Francisco in the early 1890s (Wood
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1892). Since that time, it has spread across much of
the United States and parts of southern Canada, with
occurrences in at least 27 states plus Quebec (Jokinen
1982, http://nas.er.usgs.gov). Limited published literature, anecdotal accounts, and our own observations suggest that it can reach extremely high
densities in systems where it occurs. Due to its wide
distribution and high densities, some authors have
speculated that it might have significant impacts in
invaded systems (Bury et al. 2007), and experimental
studies indicate it can negatively affect native gastropods (Johnson et al. 2009). However, very little is
known about the distribution of B. chinensis within
invaded regions, and no study has attempted to
quantify its impacts in invaded ecosystems.
In this study, we surveyed snail assemblages in 44
lakes in a region known to be invaded by B. chinensis.
We sought to describe the patterns and determinants of
B. chinensis distributions, and to assess whether
invasions of B. chinensis have altered the composition
of native snail assemblages. Because impacts of
invasive species may be localized or widespread, and
may occur rapidly or gradually, we considered multiple spatial and temporal scales in our analysis. We
tested for impacts of B. chinensis on native snails at
both the lake and site (within lake) scale, and combined
our own data with historical survey data from the 1930s
to test whether contemporary assemblage structure or
long-term changes in assemblages were related to the
occurrence or abundance of B. chinensis.
Methods
Study system
We surveyed snail assemblages in lakes of the
Northern Highlands Lake District (NHLD), Wisconsin, USA. There are [7,500 lakes in this region,
which vary widely with regard to morphology,
chemistry, human use, and other factors (Kratz
et al. 1997; Hanson et al. 2007). These lakes are an
important cultural and economic resource, and invasive species are a primary management concern.
Recent reports indicate that B. chinensis is widely
distributed across Wisconsin and Minnesota (Jass
2004; Bury et al. 2007; Johnson et al. 2009), and
anecdotal accounts and our own observations indicate
that it has been present in some lakes in the NHLD
Distribution and community-level effects of the Chinese mystery snail (Bellamya chinensis)
since at least 2003. However, the date of first
occurrence of B. chinensis in the NHLD can be
given only generally based on current knowledge, as
some time between 1940 and 2000. The earliest
records of the species in the Great Lakes and Upper
Mississippi region are from the late 1930s and 1940s
(Mills et al. 1993; Bury et al. 2007), and the earliest
Wisconsin record is from the 1950s (Teskey 1954).
The taxonomy of introduced Bellamya in North
America is somewhat uncertain. Some authors have
recognized two species (B. chinensis and B. japonica), whereas others have argued that the two forms
are simply variants of B. chinensis. For many years,
taxonomists placed the species in the genus Cipangopaludina. We follow Smith (2000), who provided a
complete synonymy and the most recent taxonomic
revision, affirming the two-species concept and
placing the species in the genus Bellamya.
Field sampling
During the summer of 2006 we collected snails at 4–6
sites in each of 44 focal lakes. Survey lakes ranged in
surface area from 14 to 1,400 ha (median = 130 ha),
and were selected to span broad gradients of landscape position, water chemistry, human use, and other
characteristics, and to maximize overlap with lakes
where Morrison (1932) has previously described snail
assemblages. For each lake, site locations were chosen
randomly within each compass quadrant of the
shoreline, using Geographic Information System
(GIS) software (ArcGIS 9.2; ESRI, Redlands, California). At each site we placed a 20 m transect line on
the lake bottom along the 1 m depth contour. At 2 m
intervals along the transect, two snorkelers collected
all the snails from within 0.25 m2 quadrats (10
quadrats per site). They then searched the vicinity of
the transect haphazardly for 5 minutes to reduce the
likelihood that B. chinensis presence at a site escaped
detection. Sampling ceased after the fourth site if at
least 25 quadrats with non-zero snail abundances had
been sampled; otherwise, sampling continued at
alternate sites until that threshold was reached or 6
sites had been sampled. At some sites the entire 20-m
transect fell in thick macrophyte beds, precluding
effective snorkel surveys. In these cases we sampled
snails by vigorously sweeping a D-net (500 lm mesh)
through the macrophytes in two 1 m2 areas. Collected
snails were preserved in 80% ethanol. Identifications
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were made according to Burch (1989), following the
revision of Hubendick (1951) for the Lymnaeidae,
Hubendick (1955) for the Planorbidae, and Wethington and Lydeard (2007) for the Physidae. All samples
are being curated into the Illinois Natural History
Survey Mollusk Collection.
We also tested the effectiveness of a rapid
assessment protocol for detecting the presence of
B. chinensis. Two observers snorkeled around the
vicinity of the boat launch (if present) for up to 5 min
each, or until B. chinensis was found. We conducted
this rapid assessment at 27 of the focal survey lakes,
as well as at 8 additional lakes where we did not
conduct full quadrat surveys.
Statistical analyses
The raw data from our sampling consisted of
abundances (counts) for each species in each quadrat.
For most analyses we aggregated these data, as either
the summed abundance at the site level or the mean
density at the lake level. Unless otherwise noted, all
statistical analyses were conducted in the R statistical
package (R Development Core Team 2008); the
‘‘vegan’’ package was used for multivariate analyses (Oksanen et al. 2008).
We assessed the adequacy of our sampling design
in two ways. First, we used linear regression to test
for a relationship between sampling effort and lakelevel species richness. Sampling effort varied from a
minimum of 8 quadrats per lake (in lakes where all
sites occurred in dense macrophytes, and only net
sweep samples were taken) to a maximum of 60
quadrats per lake (in lakes where snails were rare or
absent, and 10 quadrats were sampled at each of 6
non-vegetated sites). Second, we developed specieseffort curves by rarefaction. Within each lake, we
constructed 500 bootstrap samples of the quadratlevel data at each possible level of sampling intensity
(from 1 quadrat up to the number actually sampled in
that lake). We plotted the mean bootstrapped species
richness against sampling effort for each lake.
We described the probability of B. chinensis occurrence in a lake using multiple logistic regression
(a generalized linear model with a logit link function).
We considered eight predictors describing lakes in
terms of their physical and chemical characteristics
(area, conductivity, and Secchi depth), potential
anthropogenic dispersal vectors (shoreline housing
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density, distance to population center, and accessibility
to boats), and the presence of other invasive species
that might interact with B. chinensis (rusty crayfish
Orconectes rusticus and banded mystery snail Viviparus georgianus). Sources and methods for these data
are described in the Appendix (Table A1—Electronic
Supplementary Material). Continuous predictor variables were log-transformed when necessary to normalize distributions, and all continuous predictors
were transformed to Z-scores. We used all-subsets
regression based on Akaike’s Information Criterion to
identify the best subsets of predictors, assessed the
significance of each term in the selected model using
likelihood ratio tests, and described the predictive
power of the model by quantifying the area under the
receiver operating characteristic curve (ROC AUC) of
sensitivity versus 1-specificity (Agresti 2002).
We also considered whether within-lake distributions of B. chinensis were related to the relative
proximity of boat launches. For all lakes where
B. chinensis was present, we calculated the shoreline
distance between each survey site and the nearest boat
launch using a Geographic Information System (GIS).
To allow comparisons between lakes of different sizes
that may have been invaded at different times, we
relativized all of the site-to-launch distances for each
lake by dividing by the maximum site-to-launch
distance for that lake. Thus all the distances for all
lakes ranged between 0 and 1. We then used logistic
regression to test the hypothesis that the likelihood of
B. chinensis presence at a site was higher for sites close
to boat launches. We excluded from this analysis one
lake where B. chinensis was present at every site.
Potential effects of B. chinensis on the native snail
assemblage were examined using multivariate analyses. First, we used non-metric multidimensional scaling (NMDS) to reduce the dimensionality of the
community data and display how dominant gradients
of variation in species composition were related to
environmental variables and to the presence and
abundance of B. chinensis. NMDS is an ordination
method that preserves the ranked-ordered distances
between sample points in ordination space by minimizing a measure of disagreement (referred to as
stress) between the compositional dissimilarities and
the distance between points in the ordination diagram
(Kruskal 1964). In the context of our study, we were
particularly interested in separating the effects on
assemblage structure due to B. chinensis from those
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due to environmental variables and other invasive
species. In our study lakes, conductivity is a primary
environmental determinant of snail assemblage structure (see Results), and the rusty crayfish (Orconectes
rusticus) and the banded mystery snail (Viviparus
georgianus) are invasive species that might also
influence snail assemblages. We therefore tested for
an effect of B. chinensis on assemblage structure while
controlling for conductivity and the presence of O.
rusticus and V. georgianus. This analysis was conducted using permutation MANOVA (perMANOVA;
(Anderson 2001), which allows for ANOVA-style
partitioning of variance among predictors when the
response is a multivariate community distance matrix.
Both NMDS and perMANOVA consider the ranked
dissimilarities in assemblage structure among locations, which we calculated using Sørensen’s (BrayCurtis) distance metric. Prior to the analyses, species
abundance data were log(x ? 1) transformed and
relativized by species maxima. NMDS ordinations
were conducted in the PC-ORD software package
(McCune and Mefford 1999), and perMANOVA tests
were performed using the ‘‘adonis’’ function in R. We
also inspected plots of the abundance of each species
versus the abundance of B. chinensis for evidence that
higher B. chinensis abundances were associated with
lower abundances of native species.
We quantified changes in lake-level snail assemblages from 1930 (prior to invasion by B. chinensis) to
the present and considered whether these changes
were related to invasion by B. chinensis. Historical
snail assemblage data were available for 30 of our
survey lakes (Morrison 1932). To make those data
comparable with our own, two differences in methods
and objectives had to be reconciled. First, advances in
freshwater gastropod systematics over the last
75 years dictated a substantial simplification of Morrison’s taxonomy. Second, Morrison’s paper focused
on compiling a list of the localities where species
where known to occur, rather than describing the snail
assemblages in lakes. The omission of a lake from his
list of localities for a species could therefore represent
merely a lack of data, rather than a true absence of that
species in that lake. To account for this we classified
snail occurrences (species-lake combinations)
recorded by Morrison as either retained (still present
in our survey of that lake) or lost (absent from our
survey of that lake), and ignored occurrences in our
own data that were not recorded by Morrison. We
Distribution and community-level effects of the Chinese mystery snail (Bellamya chinensis)
used logistic regression to test whether the likelihood
that occurrences were lost was predicted by the
current-day presence of B. chinensis. In this analysis
we controlled for other factors that might influence
the likelihood that an occurrence was lost, including
the presence of the invasive snail predator O. rusticus;
the presence of the invasive snail V. georgianus; and
contemporary shoreline housing density, an indicator
of the extent of human alteration of littoral zones,
which is the primary anthropogenic impact on these
lakes (Carpenter et al. 2007). The Morrison data and
the species synonomy that we used are available in
Tables A2 and A3 (Electronic Supplementary
Material).
Results
Sampling efficiency and snail community
composition
We collected and identified 17,516 snails representing
21 species (Table A4—Electronic Supplementary
Material). Our sampling strategy effectively represented the species membership of the snail assemblages. There was no evidence that we found more
species when effort was higher; in fact, there was a
negative relationship between species richness and
the number of quadrats sampled (F1,42 = 25.4,
P \ 0.0001, R2 = 0.38), suggesting that the adaptive
sampling strategy was effective in concentrating the
greatest effort in lakes where snails were most difficult
to find. Rarefaction analysis demonstrated that sampling effort was sufficient to find most or all of the
species present in the habitats that we surveyed. For
every lake, species-effort curves reached an asymptote
at or near the species richness that we observed in our
samples, often at a sampling intensity less than the
number of quadrats that we actually surveyed in the
lake (Fig. A1—Electronic Supplementary Material).
Species abundances were approximately log-normally distributed, with a few very abundant species
and many rare species. For instance, the two most
numerically-dominant species (Amnicola limosa and
Marstonia lustrica) comprised 66% of total abundance. Lake-level species richness ranged from 0
(Camp Lake and Crystal Lake) to 14 (Allequash Lake
and Tomahawk Lake). The best model describing
species richness, selected by AIC using all-subsets
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regression, included Secchi depth and conductivity
but not log(area), B. chinensis presence, O. rusticus
presence maximum depth, or an indicator for whether
only vegetated sites were sampled in the lake
(richness = -0.75 9 Secchi ? 0.05 9 conductivity ?
6.0; P \ 0.0001, R2 = 0.45).
Distribution of B. chinensis within
and among lakes
B. chinensis was widely distributed across the study
region (Fig. 1). Of the 42 focal lakes in which snails
were present, we observed B. chinensis in quadrat
samples in 15 lakes, and during haphazard searching
near quadrats in an additional 6 lakes. We also
observed B. chinensis in 2 of the 8 lakes where only
the rapid assessment protocol was conducted. The
rapid assessment protocol was fairly effective, identifying B. chinensis presences at 9 of 12 lakes where
it was used in conjunction with regular quadrat
sampling and where B. chinensis was detected by
either method.
There was a strong geographic pattern in
B. chinensis occurrences, with the likelihood that a
lake was invaded much higher in the south than in the
north of the study region (Fig. 1). Invaded lakes in
our survey occurred in the Chippewa River and
Wisconsin River portions of the Mississippi River
drainage basin and not in the Lake Superior basin.
However, we have observed B. chinensis in lakes in
the Superior basin that were not among the 3 lakes in
that basin that we surveyed here (Johnson et al.
2009). The best model (AIC = 59.9) describing B.
chinensis presence indicated that it was more likely to
occur in lakes that were closer to a population center,
or that had higher shoreline housing density or lower
water clarity (Table 1). This model had good predictive power (area under the receiver operating characteristic curve = 0.83), illustrating a correct
classification rate of 78 % (based on a decision
threshold of 0.5). Good alternative models either
added a positive conductivity term to those listed
above (AIC = 60.1) or selected the conductivity term
in place of the Secchi depth term (AIC = 61.0).
When present, B. chinensis was patchily distributed within lakes. In all but one of the fifteen lakes
where we detected B. chinensis in quadrat sampling,
it occurred in between 2% and 56% of quadrats
(mean 15% ± 16% SD), and mean densities ranged
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C. T. Solomon et al.
Fig. 1 Map of the Northern
Highlands Lake District,
showing lakes where the
Chinese mystery snail
Bellamya chinensis was
present (lakes filled in
black) and absent (lakes
outlined in black). Lakes in
grey were not surveyed
between 0.16 and 4.00 individuals m-2 (mean
0.81 ± 1.04 SD). Otter Lake was a clear exception
to this pattern; in this lake, B. chinensis was present at
all four surveyed sites, and in 15 of 16 (94%) of
quadrats. The mean density of B. chinensis in Otter
Lake was 38 individuals m-2. Multiplying these
densities by an estimate of the mean biomass of
B. chinensis (mean ± SD of dry tissue mass excluding shell was 0.27 ± 0.15 g for a random sample of
30 B. chinensis collected from Allequash Lake in
2004; Solomon unpubl. data) yields biomass
estimates of 10.33 g dry mass m-2 in Otter Lake
and 0.04–1.08 g dry mass m-2 in the other lakes.
Within invaded lakes, the probability that
B. chinensis occurred at a given site was higher for
sites closer to boat launches (logistic regression,
v21 ¼ 6:1, P = 0.01; Fig. 2a). There was also weak
evidence that B. chinensis was more likely to occur in
lakes with improved public boat launches than in
lakes where public access was absent or limited to
carry-in boats (Pearson’s v2 = 2.8, P = 0.09;
Fig. 2b).
Table 1 Multiple logistic regression model describing the
probability of B. chinensis occurrence in a lake
Effects of B. chinensis on native snail
assemblages
P(v2)
Estimate
SE
(Intercept)
-0.26
0.35
Secchi depth
-0.84
0.40
Distance to Minocqua
-0.71
0.37
0.04
Log (buildings km-1)
1.00
0.40
0.005
0.02
Variables were selected by AIC using an all-subsets procedure.
Estimate, point estimate for coefficient; SE, standard error of
estimate; P(v2), probability of statistical significance associated
with a likelihood ratio test of the hypothesis that the
coefficient = 0
Note: Candidate variables included those in the selected model
above, as well as log (lake area), conductivity, presence of a
public boat ramp, presence of rusty crayfish, and presence of
the invasive snail Viviparus georgianus. All continuous
predictors were Z-transformed
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High site-level densities of B. chinensis were associated with low densities of some native species
(Fig. 3). Specifically, Lyogyrus granum, the Valvata
species, the Lymnaea species, Physa acuta, and
Helisoma trivolvis tended not to occur at sites where
B. chinensis abundance was greater than between 0
and 2 individuals m-2. The three species of Lymnaea
together occurred at 19 sites where B. chinensis was
absent, but at only 3 sites where B. chinensis was
present. In contrast, there was no evidence for a
negative relationship between the site-level abundance of B. chinensis and that of its closest relatives
in these lakes, the viviparids Campeloma decisum
and Viviparus georgianus.
Distribution and community-level effects of the Chinese mystery snail (Bellamya chinensis)
A
B. chinensis absent
B. chinensis present
16
Number of sites
12
8
4
0
0.0
0.2
0.4
0.6
0.8
1.0
Relative distance to boat launch
B
Number of lakes
20
15
10
5
0
with boat ramp
without boat ramp
Fig. 2 Relationship between Bellamya chinensis occurrence
and public boat launches. a The probability of B. chinensis
occurrence at sites within lakes where it occurred was highest
for sites close to a boat launch (P = 0.01). Sites were binned
according to their relative distance to the nearest boat launch
(see text). Data are from 14 lakes where B. chinensis was
detected in quadrat sampling (excludes one lake where
B. chinensis was found at all sites). b B. chinensis was more
likely to occur in lakes with improved public boat launches
than in lakes without launches or where access was limited to
carry-in boats only (P = 0.09)
Despite the negative association between the sitelevel abundances of B. chinensis and some native snail
species, there was no evidence that B. chinensis
affected overall snail assemblage structure at the level
of either sites or lakes (Fig. 4). Total native species
richness was, if anything, higher at sites where
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B. chinensis was present (mean = 6.0, n = 20) than
at sites where only native species were present
(mean = 4.8, n = 123; t23 = 1.7, P = 0.1). Assemblage structure at the lake level was correlated with
environmental variables, particularly Secchi depth and
conductivity (Fig. 4b). Results from the perMANOVA
analysis confirmed the patterns suggested by the
NMDS ordinations; even after controlling for conductivity and for the presence of O. rusticus and
V. georgianus, there was no effect of the presence of
B. chinensis on lake-level snail assemblages (Table 2).
Similarly, while there were significant changes in
snail assemblages between the historical surveys and
our own, there was no apparent effect of B. chinensis
invasion on these changes. Many of the snail
occurrences (species-lake combinations) that were
present in the historical data were ‘‘lost’’ (that is,
were not detected by our surveys; see Fig. 5, where
most points fall below the 1:1 line). The likelihood
that an historical occurrence was lost varied among
species and families (Table 3; Fig. 5a). Species that
were rare in the historical data (particularly lymnaeids, ancylids, and valvatids) often were not detected
in any of the lakes that they historically occupied
(Fig. 5a), although two of these (Valvata sincera and
Promenetus exacuous) were detected in lakes that
they had not been recorded in historically. The
likelihood that an historical occurrence was lost did
not vary as a function of present-day shoreline
housing density, of main effects of the presence of
B. chinensis, O. rusticus, or V. georgianus, or of
interaction terms of those main effects with species
(Table 3; Fig. 5b).
Discussion
Distribution of B. chinensis
The results of our regional survey and the findings of
Bury et al. (2007) for Minnesota demonstrate that
B. chinensis occurs frequently within invaded
regions, besides being widely distributed across the
United States (Jokinen 1982, http://nas.er.usgs.gov).
In the Northern Highlands Lake District of Wisconsin, B. chinensis occurred in 50% of the 42 lakes in
which we detected any snails with our full sampling
protocol, making it among the most frequently
occurring species in our study. Furthermore, the
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C. T. Solomon et al.
1000
Vivgeo
Camdec
Amnlim
Amnlus
Lyogra
Valtri
Valsin
Lymbul
Lymcat
Lymsta
Phyacu
Phygyr
Helanc
Helcam
Heltri
Proexa
Gyrpar
Gyrdef
Ferpar
Ferriv
100
10
Species abundance + 1
1
1000
100
10
1
1000
100
10
1
1000
100
10
1
1
10
100
1
10
100
1
10
100
1
10
100
1
10
100
B. chinensis abundance + 1
Fig. 3 Abundance of each native snail species (vertical axis)
and B. chinensis (horizontal axis) at 197 sites in 42 lakes. Note
log scale on axes. For each panel, the species plotted on the
y-axis is indicated in the top right corner. Species are Amnicola
limosa (Amnlim), Marstonia lustrica (Marlus), Lyogyrus
granum (Lyogra), Valvata sincera (Valsin), Valvata tricarinata
(Valtri), Bellamya chinensis (Belchi), Campeloma decisum
(Camdec), Viviparus georgianus (Vivgeo), Ferrissia parallela
(Ferpar), Ferissia rivularis (Ferriv), Lymnaea bulimoides
(Lymbul), Lymnaea catascopium (Lymcat), Lymnaea stagnalis
(Lymsta), Physa acuta (Phyacu), Physa gyrina (Phygyr),
Gyraulus deflectus (Gyrdef), Gyraulus parvus (Gyrpar),
Helisoma anceps (Helanc), Helisoma campanulata (Helcam),
Helisoma trivolvis (Heltri), and Promenetus exacuous (Proexa)
strong south-to-north pattern in occurrences and the
link between occurrences and boat launches suggest
that this species has not yet reached all of the lakes in
the NHLD in which it could potentially persist. While
our focal lakes were selected with some bias towards
lakes where previous studies had observed snails,
they were otherwise broadly representative of lakes in
the region. It may therefore be reasonable to expect
that 50% or more of the accessible lakes in this region
are or could be invaded by B. chinensis. In comparison, maximum potential distributions of many
aquatic invasive species seem to be near or below
half of the lakes in a region. For instance, 41% of 179
Minnesota lakes were estimated to be susceptible to
invasion by spiny water flea Bythotrephes longimanus (Branstrator et al. 2006), 55% of 8,110 Ontario
lakes and 11% of 5164 Wisconsin lakes were estimated to be susceptible to invasion by rainbow smelt
Osmerus mordax (Mercado-Silva et al. 2006), and
9.9% of 3908 Wisconsin lakes are deemed environmentally suitable for rusty crayfish Orconectes rusticus (Olden, unpubl. data). In regions where it occurs,
B. chinensis may be among the most ubiquitous of
invasive aquatic animals.
An important research need for managing any
invasive species is to identify which systems are
susceptible to invasion. Our analyses indicated that
the likelihood of B. chinensis occurrence was influenced both by intrinsic properties of lakes (Secchi
depth and conductivity) and by human activities
(distance to population center, shoreline housing
density, and boat launches). Apparent relationships
between environmental characteristics and the occurrence of B. chinensis should be interpreted with
caution given the suggestion above that this species
has not yet saturated the landscape in the NHLD
(Peterson 2003). With that caution in mind, we
discuss below what general properties of lakes
123
Distribution and community-level effects of the Chinese mystery snail (Bellamya chinensis)
A
Axis 2 (22.3% of variation)
Table 2 perMANOVA tests of hypothesized factors influencing snail assemblage structure, using lake-level data
df
F
P
1
0.91
3.06
\0.001
O. rusticus
1
0.36
1.21
0.24
V. georgianus
1
0.22
0.75
0.76
B. chinensis
1
0.29
0.97
0.47
37
10.96
Interaction terms are excluded for simplicity; none were
significant (all P [ 0.4). df, degrees of freedom; SS, sums of
squares; F, pseudo-F statistic for the perMANOVA test; P,
probability of statistical significance (based on 1,000 permutations
of the data) associated with a test of the hypothesis that there is no
effect of a predictor. Terms for species are presence-absence of
three invasive species: Orconectes rusticus (rusty crayfish),
Viviparus georgianus (banded mystery snail), and Bellamya
chinensis (Chinese mystery snail)
B
secchi
SS
Conductivity
Residual
Axis 1 (25.9% of variation)
Axis 2 (21.5% of variation)
1599
cond
Axis 1 (41.7% of variation)
Fig. 4 Non-metric multidimensional scaling (NMDS) of snail
assemblage data, showing the two axes (of three total) that
explained the most variation in assemblage structure in each
ordination. a Points represent assemblage structure at the site
level (143 sites in 42 lakes) for sites where B. chinensis was
absent (empty circles) or present (filed circles; diameter of
circle proportional to log(abundance) of B. chinensis at the
site). Final stress = 0.20. b Points represent assemblage
structure at the lake level (42 lakes). Symbols as in (a).
Radiating lines indicate the direction and strength of correlations between ordination axis and environmental variables that
explained[10% of the variation along any axis (secchi, Secchi
depth, and cond, conductivity). Ordination has been rotated to
maximize the correlation between conductivity and Axis 1.
Final stress = 0.14
ecosystems may increase their susceptibility to
B. chinensis invasion.
The relationships between B. chinensis occurrence
and lake conductivity and Secchi depth may indicate
an affinity for more productive systems, and/or
minimum Ca requirements for shell growth. Both
Secchi depth and conductivity are correlated with
lake productivity, and more productive systems may
allow greater snail species richness (and greater
likelihood of B. chinensis occurrence) because of
greater food availability (Dillon 2000). Conductivity
is also strongly correlated with Ca concentration in
these lakes (e.g., Johnson et al. 2008). Calcium
requirements for B. chinensis are likely to be high due
to its large shell, and Ca limitation has been
suggested to be a primary determinant of occurrence
for other invasive mollusks (e.g., Whittier et al.
2008). A survey of [200 Connecticut water bodies
found B. chinensis only in those with Ca concentrations [5 mg l-1, even though 75% of the waters
surveyed had Ca concentrations lower than that
threshold (Jokinen 1982). We found B. chinensis in
some systems that likely had Ca concentrations
\5 mg l-1 (based on the relationship between conductivity and Ca in 50 NHLD lakes; data not shown),
but nonetheless the positive relationship between
conductivity and the likelihood of B.chinensis occurrence could indicate a Ca limitation effect. It is also
important to note that conductivity is correlated with
many important properties of lakes in this region
(Kratz et al. 1997), and so its relationship with
B. chinensis occurrence could be masking the effects
of other factors. For instance, lakes with high
conductivity may also be those most frequently
visited by boaters, since they tend to be large and
support recreational fishing opportunities (ReedAndersen et al. 2000).
The relationships between B. chinensis occurrence
and distance to population center, shoreline housing
density, and boat launches indicate that greater
human use of a lake is associated with a higher
123
1600
C. T. Solomon et al.
A
Table 3 Results from a multiple logistic regression describing
the likelihood that species occurrences (species-lake combinations) recorded by Morrison (1932) were lost (i.e., were not
detected in our surveys)
Hydrobiidae
Valvatidae
Viviparidae
Ancylidae
Lymnaeidae
Physidae
Planorbidae
20
df Deviance Likelihood P (v2)
ratio
Shoreline housing
density
10
Current occurrences
Species
0
B
10
B.c. 0,
B.c. 0,
B.c. 1,
B.c. 1,
20
O.r. 0
O.r. 1
O.r. 0
O.r. 1
0
10
Historical occurrences
Fig. 5 Our surveys detected some but not all of the snail
occurrences (species-lake combinations) recorded by Morrison
(1932). a Number of lakes in which a species was found in our
surveys plotted against number of lakes in which it historically
occurred. Symbols are coded to indicate the family to which
each species belongs, including both prosobranchs (solid
points) and pulmonates (hollow points). b Number of species
found in a lake in our surveys plotted against number of species
historically found there. Symbols are coded according to the
presence (1) or absence (0) of the invasive species Bellamya
chinensis and Orconectes rusticus. Size of symbols is
proportional to present-day shoreline housing density at each
lake. Solid line indicates 1:1 relationship in each panel
likelihood of B. chinensis establishment. The link
between boat launches and within-lake distributions
of B. chinensis suggests that boater movements in
particular play an important role in dispersal. Boats
are an important vector of spread for many aquatic
invasive species, and previous studies have observed
correlations between patterns of boater movement
and lake-level occurrences of invasive species (e.g.,
123
24 277.2
83.73
0.2
\0.0001
1 193.5
0.001
1.0
V. georgianus
1 193.5
0.013
0.9
B. chinensis
1 193.6
0.067
0.8
17 165.6
19.0
0.3
Species 9 V. georgianus 16 162.6
16.1
0.4
Species 9 B. chinensis
16.8
0.6
19 163.4
The full model was focused on identifying effects of the
invasive Chinese mystery snail Bellamya chinensis on the
likelihood of loss. We controlled for among-lake differences in
human alterations to littoral zone habitat (as indicated by logtransformed shoreline housing density); for differences among
native snail species; for possible effects of the invasive crayfish
Orconectes rusticus and the invasive snail Viviparus
georgianus; and for the possibility that the effects of the
invasives on the natives varied among natives. The table gives
the degrees of freedom (df), deviance, likelihood ratio, and
probability of statistical significance (P) for likelihood ratio
tests of the significance of each term in the model
10
0
1.66
O. rusticus
Species 9 O. rusticus
0
1 148.2
Buchan and Padilla 1999; MacIsaac et al. 2004).
B. chinensis individuals will attach to macrophytes
that could get tangled on boat trailers, and we have
observed individuals brought into boats inadvertently
with sediments on anchors. The ability of B. chinensis
to close its operculum probably makes it fairly
resistant to desiccation once on a boat or trailer; that
trait, and the fact that it bears live young which may
be ‘‘stored’’ for long periods inside the adult, could
facilitate invasions even when boaters do not visit
new lakes on the same day. Intentional releases from
aquaria and water gardens and dispersal along stream
corridors could also spread B. chinensis to new lakes.
We are not aware of previous studies that have
linked within-lake distributions of invasive species to
boat launches, as our results do for B. chinensis. Yet
this pattern may be common for animal and plant
species with limited mobility, as spread around a lake
may take years after establishment at an invasion point
(Wilson et al. 2004). If rates of spread were available,
this information would allow dates of invasion to be
back-calculated in cases where species had not yet
established throughout the lake. Furthermore, the
Distribution and community-level effects of the Chinese mystery snail (Bellamya chinensis)
strong link between boat launches and localized
distributions of B. chinensis raises an interesting
hypothesis. If boater movements play such an important role in determining the distribution of B. chinensis,
it seems reasonable to expect that they could also affect
the distribution of native snails. It might be interesting
to ask whether entire snail assemblages in these lakes
are to some extent structured by patterns of human
movement across the landscape.
B. chinensis impacts on native snail assemblages?
Evidence that B. chinensis invasions influenced
native snail assemblages varied with the spatial scale
of analysis. At the whole-lake scale, neither the
contemporary data nor the historical comparison
showed any effects of B. chinensis on the presence
or abundance of native snails. These results are
consistent with the idea that invasive species rarely
extirpate their competitors (Davis 2003; Sax et al.
2007). At the more local scale of sites, the abundance
of B. chinensis was negatively associated with that of
several native species. This pattern might result from
competitive effects, but might simply reflect differences in niche requirements. Teasing apart these
alternative explanations is a notoriously difficult
problem in community ecology, although controlled
experiments can sometimes shed light on patterns
observed in the field. A recent mesocosm experiment
demonstrated that B. chinensis at densities *10
individuals m-2 had stronger effects on Lymnaea
stagnalis (reduced survival) than on Physa gyrina
(reduced growth) (Johnson et al. 2009). In our
surveys, L. stagnalis (but not P. gyrina) was one of
the species that did not occur at high abundance at
sites where B. chinensis was present (Fig. 3). This
qualitative agreement between experimental and
observational results lends some support to the idea
that B. chinensis has had negative effects on at least
some of the species with which it is negatively
associated. On the other hand, any such effects are
relatively subtle, in that no B. chinensis effect on
overall assemblage structure at the site level was
detectable (Fig. 4b). On balance our results provide,
at most, weak evidence that B. chinensis negatively
impacts native snails.
Why do we not see strong evidence that B. chinensis
invasion has negative effects on native snail popula-
1601
tions? At least three explanations are plausible. First, it
could be that insufficient time has elapsed since
invasion to detect the effects of what are in fact strong
competitive interactions (Strayer et al. 2006). This
explanation seems fairly unlikely given that no
B. chinensis effects were observed in the re-survey
analysis. However, the temporal perspective gained
from that analysis goes back only as far as the invasion
of a given lake, and it is possible that some of our
survey lakes were invaded relatively recently. Furthermore, the re-survey analysis can only detect
B. chinensis effects if they result in lake-wide extirpation of a native, whereas significant impacts could
occur below that threshold. Indeed, a second explanation for the lack of strong evidence for a negative
impact is that the impacts are not strong, but rather are
weak and localized.
Finally, of course, it could be that B. chinensis
simply does not compete with native snails. This
would suggest either resource partitioning among the
species or that resources are not limiting. Resource
partitioning seems unlikely; all of the snails collected
in our survey were co-occurring at fine spatial scales,
suggesting minimal potential for diet specialization
given that most snails seem to consume diet items
unselectively within the constraints imposed by
habitat selection (Dillon 2000). Some members of
the Viviparidae will filter feed from the water
column, but stable isotope ratios of B. chinensis
collected from one of our study lakes suggest heavy
reliance on benthic resources and little if any reliance
on pelagic resources (C. Solomon, unpubl. data). If
these species are indeed generalized deposit feeders,
then a quick glance at the lake bottom supports the
hypothesis that resources are not limiting: in most
locations in most lakes in the NHLD, an ample layer
of organic detritus mixed with periphyton covers the
bottom. This provides an interesting contrast with
some stream ecosystems where the invasive New
Zealand mud snail (Potamopyrgus antipodarum)
reaches biomasses up to 10–30 g ash-free dry
mass m-2 and appears to reduce production of native
invertebrates by appropriating much of the available
primary production (Kerans et al. 2005; Hall et al.
2006). Differences between streams and lakes in the
size of organic matter pools may help to explain this
apparent difference in the effects of B. chinensis and
P. antipodarum.
123
1602
Structure of snail assemblages
What factors do control snail assemblage structure in
this region? Of those that we considered, conductivity
and Secchi depth were the most important (Fig. 4b).
Increased availability of food (via greater primary
production), increased availability of Ca for shell
growth, and increased connectivity to dispersal corridors in drainage lakes with higher conductivity are all
possible explanations for these effects. A number of
studies have identified similar patterns, particularly
between species richness and these indicators of lake
ion content and productivity (Dillon 2000). Other
factors identified as important determinants of snail
assemblage structure in previous studies include
habitat diversity (Aho 1966; Harman 1972; Bronmark
1985), predators (Lodge et al. 1987), and dispersal
(Bronmark 1985; Lewis and Magnuson 2000; Heino
and Muotka 2006). We did not consider the effects of
habitat diversity, but we did consider the effects of at
least one important snail predator, the invasive rusty
crayfish Orconectes rusticus.
Correlative studies, small-scale experiments, and
multi-year monitoring of lakes invaded by rusty
crayfish have shown that they have strong effects on
the abundance of snails (e.g., Lodge et al. 1994; Lodge
et al. 1998; McCarthy et al. 2006). However, we found
no evidence that the presence of rusty crayfish
influenced contemporary snail assemblages or the
likelihood that historical species occurrences were lost
from lakes (Table 3). Similarly, a recent study comparing current snail abundances in lakes with and
without rusty crayfish to abundances measured in the
1930s found only weak evidence of an effect (Rosenthal et al. 2006). These apparently contradictory results
may indicate that transient dynamics imply stronger
impacts than are eventually manifested; alternatively,
they may indicate the importance of context (e.g., lakespecific densities of rusty crayfish populations) in
determining the outcome of an invasion. Either way,
they illustrate the importance of a nuanced and a longterm perspective for understanding the impacts, if any,
of non-native species (Strayer et al. 2006).
Many of the snail occurrences recorded by Morrison (1932) were not observed in our surveys.
Regardless of whether species were rare or common
in Morrison’s data, they occurred in fewer lakes in our
surveys than they did in the historical data (Fig. 5).
This is not attributable to insufficient sampling, as
123
C. T. Solomon et al.
rarefaction analyses demonstrated that we detected
most or all of the species present in the habitats that
we surveyed. However, it is possible that Morrison’s
data include species that rarely occur at 1 m depth,
where our surveys were conducted. For instance,
some of the species that were recorded by Morrison
but not in our surveys, such as Planorbula armigera
and some of the Lymnaea, are typical of small
stagnant water bodies (Baker 1928). As one simple
way to control for this potential bias, we repeated our
analysis of these data after excluding species that we
rarely observed in our surveys (i.e., those found in
\10% of the 30 lakes in the data set). The results (not
shown) were very similar to those obtained for the full
data set (Table 3); that is, even when we considered
only those species that we frequently detected in
lakes, there were no significant effects of species
invasions or shoreline development on the likelihood
that species occurrences were lost from these lakes. It
is possible that inconsistent identification of species
(not just changes in nomenclature, which we
accounted for) contributed to the apparent changes
in assemblages, although it is hard to imagine how this
could produce the patterns that we observed. Further
research is needed, perhaps employing paleoecological techniques, to clarify the patterns and understand
the drivers of the significant changes in snail assemblages that seem to have occurred in this region.
Future research
Given the widespread distribution of B. chinensis
across the United States, the lack of information
about its potential ecological impacts to date is
striking. Our results suggest that B. chinensis at the
densities that we observed has few impacts on native
snail assemblages in the study lakes that we examined. However, our results also demonstrate that this
species may be very widespread within some lake
districts, and may occur at very high biomass in
invaded lakes. In comparison to our estimate that
B. chinensis biomass is 0.04–1.08 g dry mass m-2 in
most of the invaded lakes we surveyed, the total
biomass of benthic insects at a similar depth in
nearby Crampton Lake is *1.2 g dry mass m-2
(Babler et al. 2008). Furthermore, B. chinensis may
occur at higher densities than we observed here. Thus
this species may be a significant component of the
benthic community in many lakes where it occurs.
Distribution and community-level effects of the Chinese mystery snail (Bellamya chinensis)
Further study of the impacts of this species on lake
biota and processes is therefore probably warranted.
Experimental evidence indicates that B. chinensis
may alter algal biomass and nutrient cycling in the
benthic community (Johnson et al. 2009). The
importance of benthic processes for structure and
function in lake ecosystems (Schindler and Scheuerell 2002; Vadeboncoeur et al. 2002) suggest that
alterations of these processes by B. chinensis could
have far-reaching consequences for invaded lakes,
which might suggest further management action
targeted at this species. Alternatively, if B. chinensis
has no appreciable effect on these processes, it might
be considered to be a relatively benign invasive
species, allowing management dollars to be targeted
on invasive species that do have clear negative effects
(Vander Zanden and Olden 2008). Distinguishing
between these alternatives is an important priority for
further research on this species.
Acknowledgments We thank K. Langree and E. VennieVolrath for conducting the surveys. T. Kratz and the Trout
Lake Station staff supported the field work in a number of
ways, and conducted the regional surveys from which we
derived some of our data. B. Fahey and S. Jones provided
helpful statistical suggestions, L. Kursel and J. Maxted assisted
with statistical and GIS analyses, and J. Jass provided
information about occurrence records. This work was funded
by an NSF Graduate Research Fellowship to C. Solomon, by
grants from the Department of Zoology and the Center for
Limnology at the University of Wisconsin (including a Carl A.
Bunde award, an Anna Grant Birge award, and a Juday
fellowship), by the Wisconsin Department of Natural
Resources, and by the North-Temperate Lake Long-Term
Ecological Research (NTL-LTER) Program.
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